Abstract

The life cycle of European eel (Anguilla anguilla), a catadromous species, is complex and enigmatic. In nature, during the silvering process prior to their long spawning migration, reproductive development is arrested, and they cease feeding. In studies of reproduction using hormonal induction, eels are equivalently not feed. Therefore, in female eels that undergo vitellogenesis, the liver plays different, essential roles being involved both in vitellogenins synthesis and in reallocating resources for the maintenance of vital functions, performing the transoceanic reproductive migration and completing reproductive development. The present work aimed at unravelling the major transcriptomic changes that occur in the liver during induced vitellogenesis in female eels. mRNA-Seq data from 16 animals (eight before induced vitellogenesis and eight after nine weeks of hormonal treatment) were generated and differential expression analysis was performed comparing the two groups. This analysis detected 1,328 upregulated and 1,490 downregulated transcripts. Overrepresentation analysis of the upregulated genes included biological processes related to biosynthesis, response to estrogens, mitochondrial activity and localization, while downregulated genes were enriched in processes related to morphogenesis and development of several organs and tissues, including liver and immune system. Among key genes, the upregulated ones included vitellogenin genes (VTG1 and VTG2) that are central in vitellogenesis, together with ESR1 and two novel genes not previously investigated in European eel (LMAN1 and NUPR1), which have been linked with reproduction in other species. Moreover, several upregulated genes, such as CYC1, ELOVL5, KARS and ACSS1, are involved in the management of the effect of fasting and NOTCH, VEGFA and NCOR are linked with development, autophagy and liver maintenance in other species. These results increase the understanding of the molecular changes that occur in the liver during vitellogenesis in this complex and distinctive fish species, bringing new insights on European eel reproduction and broodstock management.

Highlights

  • The life cycle of European eel (Anguilla anguilla), a catadromous species, is complex and spans a wide range of geographical areas with highly diverse habitats

  • Induced vitellogenesis of female European eel resulted in differential expression of genes involved in response to estrogen and reproduction, allowing gonad and oocyte development

  • Since eels do not feed during this process, several differentially expressed genes were linked with the requirement of energy and metabolite reallocation, several of which were differentially expressed during fasting in other species

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Summary

Introduction

The life cycle of European eel (Anguilla anguilla), a catadromous species, is complex and spans a wide range of geographical areas with highly diverse habitats. European eels spend several life stages from glass eel to yellow eel, the so-called continental-phase, in freshwater and coastal areas of Europe and northern Africa, for a period ranging from 5 to 20 years [1]. After this period, a process called silvering prepares the future spawners (silver eels) for their oceanic reproductive migration that will lead them to their spawning areas in the Sargasso Sea [2,3]. European eels need to reallocate and use accumulated reserves for the migration to their spawning areas and their reproductive development

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